A left head turn CR to a symmetric CS was found in a majority of the cats in Study I. By contrast, in Study II, a head turn towards the asymmetric CS developed. In Study III, the acquisition of these apparently conflicting CRs was directly addressed by administering the CSs asymmetrically
although presenting the CS+ and CS- to each ear equally over presenta
tions. It was reasoned that even if there might be some small differences between the left and right ear tones, those differences would not be apparent when the tones were presented separately. Therefore, tones of different frequencies were used as CS+ and CS-. The CS+ and CS- tones were presented alternatively to the left and right ear in random order.
Two contradictory predictions were formed. Based on the results of Study I, it was predicted that the cats would develop lateralized movements biased in one direction independently of the actual ear to which the CS+
tone was presented. According to the results of Study II, it was predicted that the cats would develop a head turn CR toward the particular ear to which the tone CS+ was presented.
In Studies I and II, no differences at all were found between cats stimulated in the left or right MFB. Therefore, in the present experiment the brain stimulation was always applied to the right MFB. It was expected that when all the cats were stimulated on the same side of the brain, a larger group would be made available for the analysis of the evoked potential responses recorded in the cingulate cortex ipsi- and contralateral to the brain stimulation US.
Methods
Adult cats were used in the study. During the CS test session, and during the subsequent four conditioning sessions, 1000 and 2500 Hz tones were presented either to the left or right ear at an equal intensity and in ran
dom order. One randomly selected tone (1500 ms, either 1000 or 2500 Hz) was used as the CS+ and the other tone as the CS-. The CS+ tone was presented randomly to either left or right ear, and it overlapped during the last 500 ms with the stimulation US. CS- trials consisted of the presen
tation of the other tone randomly either to the left or right ear. All the stimulation electrodes were implanted in the right MFB. Movements and evoked responses were analyzed in 12 animals.
Results
During the CS test session, all the cats initially moved their heads in response to the tones. Analysis of the direction of the orienting head turns before habituation showed that 11 out of 13 cats predominantly turned their heads in the direction of the tone. Regardless of the ear to which the tone was presented, two cats more often preferred to turn their heads ipsilateral (i.e. to the right) than contralateral to the side of the right MFB
stimulation electrode. The habituation rate of the head movements to the tones presented ipsi- and contralateral to the stimulation electrode was equal.
During the final conditioning session, the responses to the CS+
tones were rapid head turns, without any other body movements. The head movements to the CS- tones were slower, they had a longer onset latency, and the displacement of the head was not as great as to the CS+
tones. Three cats turned in the actual direction of the CS+ and CS- tones.
Ten cats, however, turned in one direction in response to the CS+ and CS
tones, regardless of the direction from which the tones were presented.
Two of the cats that had turned ipsilateral to the side of the stimulation electrode during the CS test session continued with this response ten
dency during conditioning. Eight other cats showed unilateral CRs, although they had turned toward the tone during the CS test session.
Two of these cats turned ipsilateral, and six contralateral, to the US in response to the CS presentations. Thus, those cats which during condi
tioning did not retain the bilateral orienting movements observed during the CS test session more frequently turned contralateral than ipsilateral to the US.
The head movement UR evoked by the US was not related to the head turn CR. A left head turn UR was observed in three cats; in one of these cats, the head turn CR was also to the left, but in one other cat, it was to the right. A head movement UR upwards or forwards was found in 10 cats, two of which also showed a slight bias to the right.
Both head movement onset latencies and accelerations were different in response to the CS+ and CS-. The head movement accelera
tion furthermore increased over sessions only in response to the CS+.
Whereas negative evoked potential deflections were equal in the cingulate cortex ipsi- and contralateral to the US electrode in the first conditioning session, during subsequent sessions the negativity was greater in the ipsilateral cingulate cortex. While in the contralateral cingu
late cortex no differences in response to the CS+ and CS- were observed, in the ipsilateral cingulate cortex the negativity was larger in response to the CS+ than CS-, and this difference increased over sessions.
The relationship between cingulate cortex evoked potentials to MFB stimulation during the US test session, and to the CS+ during the final conditioning session, was analyzed by computing product moment correlations between the US and CS+ waveforms in the cingulate cortices ipsi- and contralateral to the MFB stimulation. This analysis was per
formed for nine animals with artifact-free US recordings. The evoked potential waveforms of the CS+ and US averages were similar to each other in both the ipsi- and contralateral recordings. This indicates that the form of the CS+ evoked potential responses closely corresponded to the
form of the US evoked potential responses. In five cats, the ipsi- and con
tralateral cingulate cortex CS+ evoked potential waveforms were rather similar. In these cats, negative evoked potential deflections appeared in both sides of the brain in response to both the US and CS+, but were generally smaller in the contralateral than ipsilateral cingulate cortex. In four other cats, the CS+ waveforms between the two sides of the brain did not resemble each other. In these cats, a predominantly negative deflection was observed in the cingulate cortex ipsilateral to the US but a positive deflection in the cingulate cortex contralateral to the US. Taken together, in the ipsilateral cingulate cortex the US appeared to evoke negative potentials, and this negativity was recorded as a similar CS+
evoked potential response during the final conditioning session. Corre
spondingly, in the contralateral cingulate cortex, the US evoked a smaller negativity and even positivity, and the CS+ evoked potentials resembled these potentials during the final conditioning session.
Discussion and conclusions
In the present study the cats showed conditioned behavioral discrimina
tion to the CS tones. This differentiation appeared as orienting head turns, that were more extended, of greater acceleration, and of shorter onset latency to the CS+ than to the CS-.
The present finding that a majority of the cats showed lateralized head movement CRs during the conditioning session corresponds to the findings of Study I, where symmetrical presentation of the CS+ resulted in lateralized responding. The present experiment specifically showed that lateralized movements appeared even though the CS+ was presented asymmetrically but with equal intensity and probability to each ear.
Because the asymmetric CS+ was presented in a balanced sequence across the ears, the lateralization of the orienting head movements did not develop due to physical or perceived asymmetries of the CS+ as in Study II. Furthermore, some initial preference in orienting ipsi- or contralateral to the side of the US did not cause lateralization of the CRs, as no initial preference was found during the CS test session.
The appearance of lateralized orienting movements in response to the CS+ suggests that the pairing of the CS+ with unilateral MFB stimu
lation might have induced asymmetric changes in the brain structures involved in the neural control of auditory orientation. The imbalance in the neural activity between bilateral structures, usually with a greater activation of structures contralateral to the ear to which the tone is presented, is thought to be responsible for sound localization (Masterton
& Imig, 1984). The pairing of the asymmetric CS+, presented to both ears
on randomly alternating trials with MFB stimulation, may have lead to increased neural activity in the auditory structures located ipsilateral to the brain stimulation. This might have activated perceptual processes localizing the tone contralateral to the side of the US presentation, irrespective of the ear to which the tone was presented. This might explain why a head turn CR contralateral to the US was observed in the present study. Also, increased activation of ipsilateral non-auditory brain areas that control head turning may have occurred. The side of the brain contralateral to the direction of turn is believed to make a greater contri
bution to the turning response (Yeomans & Tehovnik, 1988). Thus, the neural structures involved in both sensory and motor control of orienting behavior may have exerted greater excitability ipsilateral to the US.
In Study I, a frequent CR was a head turn to the left with greater evoked potential responses in the right cingulate cortex. This was also observed in the present study, with a head turn to the left as the most frequent lateralized response. Furthermore, greater negative evoked potential deflections in the cingulate cortex ipsilateral to the MFB elec
trode means greater negative deflections in the right cingulate cortex.
These convergencies between the two studies might indicate, that although the present results were interpreted to indicate a greater neuro
nal activation in the cingulate cortex ipsilateral to the MFB stimulation electrode, the possibility exists that also the left vs. right side dichotomy might have contributed to the results.
The analysis of the evoked potential waveforms supports the possibility of selective increases in brain activity ipsilateral to a brain stimulation US. The cross-correlations indicated that in some animals the CS+ waveforms differed between the cingulate cortices ipsi- and contra
lateral to the MFB stimulation. In contrast, the CS+ and US waveforms were quite similar to each other in both cingulate cortices in all cats. This would indicate that differences between the CS+ evoked potential wave
forms between the two sides of the brain were related to differences between the brain sides in response to the brain stimulation US. Thus, due to the asymmetric effects of the US in the two cingulate cortices, the conditioned evoked potential changes were also asymmetric.
In conclusion, the present study basically showed that condition
ing was greatest when the effects of a CS presentation and US stimulation were on the same side of the brain.